International Journal of Food Microbiology 202 (2015) 35–41

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International Journal of Food Microbiology journal homepage: www.elsevier.com/locate/ijfoodmicro

Empirical prediction and validation of antibacterial inhibitory effects of various plant essential oils on common pathogenic bacteria Gulsun Akdemir Evrendilek ⁎ Department of Food Engineering, Abant Izzet Baysal University, 14280 Bolu, Turkey

a r t i c l e

i n f o

Article history: Received 19 November 2014 Received in revised form 20 February 2015 Accepted 23 February 2015 Available online 28 February 2015 Keywords: Plant essential oil Food safety Microbial inhibition GC-MS analysis

a b s t r a c t In this study, fractional compound composition, antioxidant capacity, and phenolic substance content of 14 plant essential oils—anise (Pimpinella anisum), bay leaves (Laurus nobilis), cinnamon bark (Cinnamomum verum), clove (Eugenia caryophyllata), fennel (Foeniculum vulgare), hop (Humulus lupulus), Istanbul oregano (Origanum vulgare subsp. hirtum), Izmir oregano (Origanum onites), mint (Mentha piperita), myrtus (Myrtus communis), orange peel (Citrus sinensis), sage (Salvia officinalis), thyme (Thymbra spicata), and Turkish oregano (Origanum minutiflorum)—were related to inhibition of 10 bacteria through multiple linear or non-linear (M(N)LR) models—four Gram-positive bacteria of Listeria innocua, coagulase-negative staphylococci, Staphylococcus aureus, and Bacillus subtilis, and six Gram-negative bacteria of Yersinia enterocolitica, Salmonella Enteritidis, Salmonella Typhimurium, Proteus mirabilis, Escherichia coli O157:H7, and Klebsiella oxytoca. A total of 65 compounds with different antioxidant capacity, phenolic substance content and antibacterial properties were detected with 14 plant essential oils. The best-fit M(N)LR models indicated that relative to anise essential oil, the essential oils of oreganos, cinnamon, and thyme had consistently high inhibitory effects, while orange peel essential oil had consistently a low inhibitory effect. Regression analysis indicated that beta-bisabolene (Turkish and Istanbul oreganos), and terpinolene (thyme) were found to be the most inhibitory compounds regardless of the bacteria type tested. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Recently, consumer demands have been dramatically on increase for agro-ecologically grown, fresh-like, and more nutritious foods (Saei-Dehkordi et al., 2014; Pavlović et al., 2012; Simic et al., 2004). The uses of essential oils and plant extracts have been already widespread in the pharmaceutical and cosmetic industries for the provision of flavor and fragrance. However, the use of plant essential oils has been the new focus of agricultural and food industries as an alternative to synthetic food additives for inactivation of microorganisms such as pathogenic and spoilage bacteria that cause food safety- and public health-related issues during transportation, storage, shelf-life, and packaging (Mangena and Muyima, 1999; Smith-Palmer et al., 2001). Effects of various plant essential oils tested against foodborne, plantborne and food spoilage bacteria revealed that antibacterial activity changes depending on applied dose, plant type, microorganism type, major and minor compounds in chemical compositions of plant essential oils, antioxidant capacity, total phenolic substance content, climate, and their interactions (Edris and Farrag, 2003). There are numerous in vivo and in vitro studies conducted about the bacterial inactivation and extension of shelf-life of various foods such as apples, oranges, lettuce, yogurts, meat, and bread with different ⁎ Tel.: +90 374 2532619; fax: +90 374 2534558. E-mail address: [email protected].

http://dx.doi.org/10.1016/j.ijfoodmicro.2015.02.030 0168-1605/© 2015 Elsevier B.V. All rights reserved.

essential oils (Gutiérrez et al., 2011; Jałosńska and Wilczak, 2009; Park et al., 2011; Raybaudi-Massilia et al., 2009; Singh et al., 2011). For example, essential oils of bay leaves, Spanish lavender, fennel, and Turkish oregano were reported to have different inhibitory effects on four pathogenic bacteria due to their fractional compound composition (Dadalioglu and Evrendilek, 2004). For the removal of Staphylococcus aureus from food-processing facilities, thyme and patchouli oils out of 19 essential oils were determined to be required in high concentrations in order to achieve logarithmic reductions over 4 log CFU/cm2 after a 30min exposure (Vázquez-Sánchez et al., in press). To the authors' best knowledge, however, there exists no study about empirical prediction and validation of bacterial inhibition of multiple plant essential oils. Therefore, the objectives of the present study were (1) to quantify chemical composition, total antioxidant capacity (AOC), total phenolic substance content (PSC) and (2) to model antibacterial inhibitory effects of 14 plant essential oils—anise (Pimpinella anisum), bay leaves (Laurus nobilis), cinnamon bark (Cinnamomum verum), clove (Eugenia caryophyllata), fennel (Foeniculum vulgare), hop (Humulus lupulus), Istanbul oregano (Origanum vulgare subsp. hirtum), Izmir oregano (Origanum onites) mint (Mentha piperita), myrtus (Myrtus communis), orange peel (Citrus sinensis), sage (Salvia officinalis), thyme (Thymbra spicata), and Turkish oregano (Origanum minutiflorum)—on inhibition of 10 bacteria types—four Gram-positive ones of Listeria innocua, Staphylococcus aureus, coagulase-negative staphylococci (CNS), Bacillus subtilis, and six Gram-negative ones of Yersinia enterocolitica, Salmonella

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G. Akdemir Evrendilek / International Journal of Food Microbiology 202 (2015) 35–41

Enteritidis, Salmonella Typhimurium, Proteus mirabilis, Escherichia coli O157:H7, and Klebsiella oxytoca—using the best-fit multiple linear or non-linear regression (MLR or MNLR) models.

2. Materials and methods 2.1. Bacterial cultures Listeria innocua (ATCC 33090), S. aureus (OSU 137), B. subtilis (OSU 494), Y. enterocolitica (OSU 798), S. Enteritidis (OSU 799), S. Typhimurium (ATCC 2637), E. coli O157:H7 (ATCC 35218) and isolated cultures of K. oxytoca (K-14), P. mirabilis (7002), and coagulase-negative staphylococci (CNS) (P-13) from the infected patients were obtained from the culture collection of the Department of Microbiology of the Ohio State University (Columbus, OH). The cultures were activated transferring from tryptic soy agar (TSA) slants into TSA broth and incubation at 35 ± 2 °C overnight.

2.2. Plant materials Leaves and aerial parts of Turkish oregano (O. minutiflorum), Izmir oregano (O. onites L.), Istanbul oregano (O. vulgare), and thyme (T. spicata) were obtained from Samandağ (Hatay, Turkey). Fresh bay leaves (L. nobilis) were collected from Aknehir (Hatay, Turkey). Fennel seeds (F. vulgare), mint (M. piperita), sage (S. officinalis), anise (P. anisum), clove (E. caryophyllata) cinnamon bark (C. verum), and myrtus (M. communis) were purchased from local stores in Hatay (Turkey). Orange (C. sinensis) fruits were collected from a fruit garden located in Adana (Turkey). Hop (H. lupulus) was obtained as granulated particles from a beer production company in Istanbul (Turkey). Oregano, thyme, bay, mint and sage leaves were separated from their stems, and air-dried until their use. Picked oranges were peeled and peeled shells were air-dried until their use.

2.3. Determination of major constituents of plant essential oils Air-dried parts of the plants and their seeds were steam-distilled for 3 h using a Clevenger-type apparatus (Ildam, Ankara). Essential oils thus obtained were stored in air-tight glass vials covered with aluminum foil at 4 °C. Gas chromatography (GC) mass spectrophotometer (MS) analyses of the obtained essential oils were conducted using a Shimadzu GC-MSQP2010 (Tokyo, Japan) equipped with a mass selective detector. The GC was equipped with a (5%-Phenyl)-methylpolysiloxane HP-5MS column and an AOC-20i/s automatic injection system (Tokyo, Japan). Helium was used as the carrier gas at a flow rate of 15.9 mL/s. Except for bay leaves which were mixed with diethyl ether, all the essential oils were mixed with hexane. Before the analysis, 30 μL of the oils were mixed with 1 mL of the solvent, and after the addition of anhydrous Na2SO4 to remove water; the mixture was injected into a GCMS sampling port. The chromatogram was produced holding the oven temperature at 50 °C for 5 min and then programming it from 50 to 90 °C with a 2 °C increase per min. After 90 °C, temperature was increased to 210 °C with a 5 °C-increase per 1 min. Quantification of components in the essential oils, and determination of their retention times were carried out with a Villey 275 MS data Library.

2.4. Determination of antioxidant capacity of plant essential oils Tris–HCl buffer at pH 7.4 was added to 0.1 mL of the essential oil samples, the mixture was vortexed at 2400 rpm for 8 min, and 1 mL of 2,2-diphenyl-1-picrylhydrazyl (DPPH), prepared in ethanol, was added. The absorbance of the mixture was measured at the wavelength of 517 nm (Moon and Terao, 1998).

2.5. Determination of total phenolic substance content of plant essential oils Diluted essential oil samples were filtered through a 0.45-μm filter, 5 mL of 0.2 N Folin-Ciocalteu was added to 1 mL of the filtered samples and mixed by vortexing. Then, a 4 mL of saturated Na2CO3 was added, and the mixture was placed in a water bath adjusted to 50 ± 1 °C for 5 min. Absorbance of the samples was measured at 760 nm after rapid cooling of the sample to room temperature. Obtained absorbance values were calculated from the gallic acid standard curve prepared with 100, 200, 300, 400, and 500-mg/L gallic acid. Total phenolic substance content of the samples was calculated as mg/L gallic acid-equivalence (GAE) (Spanos and Wrolstad, 1990). 2.6. Determination of antibacterial inhibitory effects of essential oils Inhibitory effects of the plant essential oils were tested using a disk diffusion assay. One milliliter of overnight-grown cultures was overlaid to plate count agar (PCA Difco, France) and spread onto agar surface. A 6 mm paper disk containing 5 μL of each essential oil was placed in the center of the petri plates which were in turn sealed with parafilm. After incubation at 35 ± 2 °C for 24 to 48 h, inhibition zone was measured and expressed in mm using a Vernier micrometer. Each experiment was repeated at least four times. 2.7. Data analysis Data were analyzed using Minitab software version 16.1 (Minitab, Inc., State College, PA). Tukey's multiple comparison tests following one-way analysis of variance (ANOVA) were performed to determine mean significant differences in inhibitory effect of the essential oils. Multiple linear or non-linear regression models were built to predict inhibition of the 10 Gram-negative and -positive bacteria as a function of plant type—a categorical variable with 14 levels and anise as the reference level—, antioxidant capacity (AOC), and total phenolic substance content (PSC). A stepwise procedure was followed using alphato-enter and -to-remove values of 0.05, a two-way interaction between AOC and PSC, and the predictors of AOC and PSC with the highest power of up to three in order to choose the best-fit MLR or MNLR models. Also, the best-fit MNLR models were constructed using a stepwise procedure with alpha-to-enter and -to-remove values of 0.001 in order to predict AOC, PSC, and inhibition of the 10 bacteria as a function of fractional composition of active compounds found in the plant essential oils. In addition to goodness-of-fit expressed in coefficient of determination (R2) or adjusted R2 (R2adj), to measure the predictive power of the best-fit MLR or MNLR models, cross-validation was conducted and results were expressed using R2CV values. Multicollinearity among predictors was measured using variance inflation factor (VIF) whose values greater than 10 indicate its presence (O'Brien, 2007). Durbin– Watson statistic for each model was used to indicate the degree of autocorrelation (serial dependence) between measurements whose values above 0.5 show the lack of auto correlation in the MLR or MNLR models (Durbin and Watson, 1971). 3. Results and discussion 3.1. Chemical compositions of essential oils A total of 65 compounds were detected for a total of 14 plant essential oils (Table 1). The compound types and their fractional composition as detected through GC-MS analyses are presented for each plant essential oil in Table 1. The compound fraction ranged from a minimum of 0.1% for spathulenol in clove, terpinen-4-ol in Istanbul oregano, for thymol in mint, for γ-terpinene in orange peel, and for β-pinene in thyme to a maximum of 90% for limonene in orange peel followed by 84% and 80% for trans-anethole in anise and fennel, respectively. The number of compounds detected for each plant essential oil varied

G. Akdemir Evrendilek / International Journal of Food Microbiology 202 (2015) 35–41

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Table 1 Compounds and their fractional composition (%) of 14 plant essential oils as determined by GCMS analyses (n = 3). Compound (%) α-pinene Camphene Sabinene 3-octanol β-pinene 1-octen-3-ol Myrcene β-myrcene α-phellandrene α-terpinene p-cymene o-cymene Limonene 1,8-cineole γ-terpinene Linalool Terpinolene α-thujone Camphor Menthone Terpinen-4-ol Borneol Neomenthol α-terpineol Iso-Menthol Methyl chavicol Estragole Anisaldehyde Pulegone Carvone (E)-cinnamaldehyde Piperitone Linalyl acetate Bornyl acetate Chavicol Thymol Carvacrol α -terpinyl acetate Neryl acetate Piperitenone oxide α-copaene Piperitenone Geranyl acetate β-cubebene Methyl eugenol Cinnamyl acetate β-caryophyllene Aromadendrene β-farnesene α-humulene β-selinene α-selinene β-bisabolene Germacrene-D Eugenyl acetate Spathulenol Caryophyllene oxide Carvacrylmethyl ether Δ-cadinene Β-cubebene Trans-anethole Methyl eugenol Anise aldehyde Trans-cinnamaldehyde Eugenol Total count of compounds

Anise

Bay leaves

1.7

6.1

Cinnamon

Clove

2.3

Fennel

Hop

3.4

Istanbul oregano 1.7 0.6

Izmir oregano 4.1

12.7

16.0

Mint

Myrtus

1.2

29.4

0.9 0.2 1.4 0.9

0.6

0.4

1.0 11.8

1.0

0.2

2.0

1.2

0.8

Thyme

Turkish oregano

0.7

1.5 0.7

0.1

0.3

0.6

0.5

0.2 1.4 8.1

1.1

0.7

1.7 8.1 2.1

1.8 2.4

3.1 9.2

3.7 60.4 1.0 0.7

0.2

Sage

1.2

2.5 12.6

Orange peel

23.5 20.1

12.6 10.4

90.1 0.1 4.1

0.5

1.4 2.4 11.5 2.4 1.8 34.7 23.5

0.3 17.8 0.2 0.2 0.6

9.1 2.4 0.5

8.0 3.2

0.1

0.9

0.2

0.2 1.2 2.0

15.7

3.1

2.0

1.4

12.8 9.1 5.1 5.0 45.1 0.9 61.1 7.4 4.8 2.7 0.3 68.2

50.9 1.5

0.1 0.4

3.4 7.4 3.3 1.0

60.5 6.6

76.4

0.5 0.3

3.8 0.7

0.2

0.2

0.3

6.9 1.3

3.5 9.1 0.8 2.9 1.6

0.4

1.4 1.5

15.7

14.7 6.8 32.6 10.5 12.7

2.5

3.4 0.3

0.4

0.8

0.2

2.3

0.2

0.2 1.2

13.0 0.1 1.0 0.9

1.2

1.1 0.8

0.6 0.5 84.0 0.5 1.2

80.4

32.2 8

0.5 10

6

67.3 8

7

8

15

between six for cinnamon and 18 for mint. Out of the 65 compounds, the three most frequently detected ones were α-pinene (86%), βcaryophyllene (64%), and linalool (57%), whereas the 39 compounds shown in Table 1 were detected only in one plant essential oil. These least detected compounds were found mostly in mint and not found in bay leaves, and Istanbul, Izmir and Turkish oreganos.

8

18

13

9

15

17

Presence (%)

RI

86 21 21 7 29 7 43 14 7 36 21 7 43 29 50 57 7 36 7 7 29 7 7 36 7 7 7 7 7 7 7 7 7 7 7 29 43 7 14 7 14 7 7 7 7 7 64 21 7 43 7 7 14 7 7 7 14 21 7 7 14 7 7 7 14

935 950 965 976 977 978 981 987 1001 1012 1015 1020 1025 1036 1060 1086 1092 1104 1144 1156 1164 1167 1170 1176 1182 1193 1197 1200 1203 1226 1247 1248 1255 1281 1287 1291 1299 1348 1365 1373 1375 1378 1379 1390 1399 1413 1420 1440 1454 1455 1486 1495 1508 1513 1521 1577 1578 1583 1601 1662 1790 2007 2015 2032 2161

16

Similar to our finding that trans-anethole (84%) was the major compound of anise essential oil, Besharati-Seidani et al. (2005) reported that Iranian anise seed contained trans-anethole (90%) as a major compound based on the headspace solvent micro extraction (HSME). Mallavarapu et al. (2004) found methyl chavicol (91.7% to 95.2%) as the major constituent of anise (Agastache foeniculum) grown in

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Bangalore (India). That 1,8-cineole (60%) was the major constituent of bay leaves oil in the present study is in agreement with 1,8-cineole (31%) as the most dominant compound of bay leaves essential oil extracted by Caredda et al. (2002) using supercritical carbon dioxide. The major compound of cinnamon bark essential oil in the present study was (E)-cinnamaldehyde (61%) and is in close agreement with (E)-cinnamaldehyde (60%) of cinnamon (Cinnamomum zeylanicum) essential oil obtained in Iran (Ojagh et al., 2010). Eugenol (68%) detected in this study as the major compound of clove essential oil is supported by similar findings reported about eugenol (78%) by Prashar et al. (2006), (48%) by Pawar and Thaker (2006), and (88.5%) by Lee and Shibamoto (2002) and Chaieb et al. (2007) for clove. Trans-anethole (80%) was identified in this study as the major constituent of fennel and was similar to that (70%) of fennel reported by Anwar et al. (2009). α-humelene (32%) as the major compound of hop essential oil found in the present study was also reported in the range of 11% to 33% for hop in five localities of Lithuania by Bernotiene et al. (2004). The major compounds of Istanbul and Izmir oreganos, and thyme were carvacrol (68%), thymol (51%), and thymol (61%), respectively. Carvacrol was found as the major component of Origanum acutidens by Kordali et al. (2008) (87%), of Thymus revolutus (an endemic species of Hatay) by Karaman et al. (2001) (43%), and of seven species of oregano (O. vulgare, O. acutidens, Origanum hypericifolium, Origanum bargyli, Origanum saccatum, Origanum solymicum, and Origanum leptocladum) by Figueredo et al. (2006) (66% to 72%). In the present study, the major constituents of mint, myrtus and orange peel essential oils were pulagone (45%), α-pinene (29%), and limonene (90%), respectively. Menthol (40%) (Mimica-Dukić et al., 2003), and α-terpinene (20%) (Yadegarinia et al., 2006) were the major compounds of essential oils of different mint species. Similarly, α-pinene (29%), and limonene (88%) were reported as the major compounds of M. communis (Yadegarinia et al., 2006) and orange peel (Lin et al., 2010), respectively. The most predominant compound of sage essential oil was α-thujone (35%). The major constituent of a different sage species was found as limonene (22%) by Bozin et al. (2007). 3.2. Antioxidant activity and total phenolic content of plant essential oils Antioxidant capacity and PSC of the 14 plant essential oils varied between 89% for Izmir oregano and 65%–66% for sage, hop, and anise and between 8.3 mg/L GAE for Izmir oregano and 4.1 mg/L GAE for anise, respectively (Table 2). In general, the oregano and thyme species had a higher AOC and PSC than did the remaining species. Similarly, Viuda-Martos et al. (2010) reported that essential oils of thyme (Thymus vulgaris) and oregano (Origanum syriacum) contained a higher AOC than did rosemary (Rosmarinus officinalis), marjoram (Majorana hortensis), lemongrass (Cymbopogon citratus) and Artemisia (Artemisia Table 2 Antioxidant capacity (AOC) and total phenolic substance content (PSC) of 14 plant essential oils (n = 3). Plant source

AOC (%)

PSC (mg/L GAE)

Anise Bay leaves Cinnamon Clove Fennel Hop Istanbul oregano Izmir oregano Mint Myrtus Orange peel Sage Thyme Turkish oregano

65.7 ± 0.6hi 74.7 ± 1.2e 72.2 ± 0.2f 69.6 ± 0.2g 66.5 ± 0.2h 65.7 ± 0.2hi 83.2 ± 0.1c 89.3 ± 0.2a 77.9 ± 0.2d 72.7 ± 0.2f 68.9 ± 0.2g 65.2 ± 0.2i 85.7 ± 0.1b 83.3 ± 0.2c

4.2 ± 0.3f 5.2 ± 0.1e 5.6 ± 0.2e 6.6 ± 0.2d 6.8 ± 0.2d 8.1 ± 0.1a 8.3 ± 0.2a 8.3 ± 0.2a 8.0 ± 0.2ab 7.0 ± 0.2cd 6.9 ± 0.1cd 5.3 ± 0.1e 7.4 ± 0.2bc 7.1 ± 0.3cd

Mean values in the same column with a different superscript letter are significantly different (p b 0.001).

annua) essential oils. Lagouri et al. (2011) found that oregano species (O. vulgare ssp. Hirtum) had the highest content of total phenolics. 3.3. Antibacterial inhibitory effects of plant essential oils The highest and lowest inhibition of the Gram-positive bacteria ranged from 90 mm for B. subtilis by thyme to 6 mm for L. innocua and B. subtilis by bay leaves, for CNS by hop, and for B. subtilis by myrtus, and orange peel. Essential oils of oregano and thyme species consistently appeared to be the most effective in the inhibition of all the Grampositive bacteria (p b 0.05) (Table 3). Relative to the other plant species, the essential oil of Izmir oregano led to the maximum inhibition of L. innocua, CNS, and S. aureus, while that of thyme resulted in the maximum inhibition of B. subtilis. Except for clove, the maximum inhibitory effect of each essential oil changed depending on the type of the Gram-positive bacteria. The essential oils of anise, bay leaves, cinnamon, orange peel, and sage exerted the most inhibitory effect on S. aureus; those of fennel, Izmir oregano, mint, myrtus, and Turkish oregano on CNS; those of hop, and Istanbul oregano on L. innocua; and only thyme essential oil on B. subtilis. As with the Gram-positive bacteria, the oregano and thyme species had the most inhibitory effects on the Gram-negative bacteria which can be attributed to the constituents such as thymol in Izmir oregano and thyme, and carvacrol in Istanbul and Turkish oreganos. Sivropoulou et al. (1996) reported that a total of 41 compounds were detected in three Origanum essential oils. However, 30, 33 and 35 compounds out of 41 were detected in commercially available Origanum oil, O. vulgare, and Origanum dictamnus, respectively. The three essential oils exhibited high levels of antibacterial activity against eight strains of Gram-positive and Gram-negative bacteria. Among the major components of the three oils, carvacrol and thymol exhibited the highest levels of antibacterial activity, while their biosynthetic precursors γ-terpinene and p-cymene were inactive. In this study, the mean difference in the degree of inhibition between the Gram-positive bacteria (26.2 ± 23.2 mm) and the Gramnegative bacteria (24.8 ± 25.4 mm) was not found to be significant (p b 0.05). The mean inhibition of the Gram-negative bacteria (Table 4) varied from 6 mm for Y. enterocolitica by fennel, mint, orange peel, and sage, for S. Typhimurium by fennel, for P. mirabilis by hop, for E. coli O157:H7 by mint, and myrtus, and for K. oxytoca by hop, and orange peel to 90 mm for Y. enterocolitica, P. mirabilis, and E. coli O157:H7 by Izmir oregano. The maximum inhibition effect of each essential oil except for anise depended on the type of the Gram-negative bacteria. Y. enterocolitica was inhibited most by bay leaves, hop, and Izmir oregano; S. Enteritidis most by clove, and fennel; S. Typhimurium most by mint, myrtus, orange peel, and sage; P. mirabilis most by Istanbul and Table 3 Halo diameter (mm) of disk diffusion assay of 14 plant essential oils against four Grampositive bacteria (n = 3). Plant source

L. innocua

CNS

S. aureus

B. subtilis

Anise Bay leaves Cinnamon Clove Fennel Hop Istanbul oregano Izmir oregano Mint Myrtus Orange peel Sage Thyme Turkish oregano

9.0 ± 2.0ghB 6.0 ± 0.01hB 21.3 ± 0.6eB 14.8 ± 2.8fA 8.3 ± 0.6ghAB 29.7 ± 0.6dA 55.6 ± 1.7cAB 69.0 ± 1.0aAB 8.0 ± 1.0ghB 7.3 ± 0.6ghB 8.2 ± 1.0ghAB 10.6 ± 0.6gAB 63.7 ± 1.2bB 54.0 ± 1.0cB

15.7 ± 0.6cdeAB 7.5 ± 0.5eAB 21.2 ± 0.3cdB 13.1 ± 0.2deA 10.2 ± 0.4deA 6.0 ± 0.01eC 27.7 ± 8.0cC 76.9 ± 9.7aA 21.5 ± 4.0cdA 16.4 ± 1.6cdeA 7.3 ± 0.6eAB 10.3 ± 0.6deB 49.9 ± 9.1bBC 70.3 ± 2.9aA

23.3 ± 5.5cA 10.8 ± 2.6dA 52.2 ± 6.0bA 11.0 ± 1.0dA 8.3 ± 0.6dB 24.4 ± 1.4cB 50.0 ± 5.0bB 71.7 ± 6.0aA 11.7 ± 0.8dB 15.8 ± 0.2cdA 8.5 ± 1.3dA 14.1 ± 1.8cdA 43.7 ± 6.5bC 44.5± 4.1bBC

9.2 ± 2.3eB 6.0 ± 0.01eB 27.9 ± 4.8dB 12.0 ± 1.0eA 6.6 ± 1.0eB 7.9 ± 1.0eC 67.5 ± 6.9bA 53.0 ± 8.2cB 9.2 ± 2.3eB 6.0 ± 0.01eB 6.0 ± 0.01eB 13.3 ± 2.1eAB 90.0 ± 0.01aA 42.3 ± 5.7cC

Mean values in the same column that do not share the same small superscript letter and in the same row that do not share the same capitalized superscript letter are significantly different (p b 0.001 for columns; p b 0.05 for rows).

G. Akdemir Evrendilek / International Journal of Food Microbiology 202 (2015) 35–41

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Table 4 Halo diameter (mm) of disk diffusion assay of 14 plant essential oils against six Gram-negative bacteria (n = 3). Plant source

Y. enterocolitica

S. Enteritidis

S. Typhimurium

P. mirabilis

E. coli O157:H7

K. oxytoca

Anise Bay leaves Cinnamon Clove Fennel Hop Istanbul oregano Izmir oregano Mint Myrtus Orange peel Sage Thyme Turkish oregano

8.7 ± 0.6eA 11.7 ± 0.6eA 17.9 ± 3.5eBC 9.7 ± 3.3eBC 6.0 ± 0.01eB 37.1 ± 3.7dA 58.3 ± 13.2bcBC 90.0 ± 0.01aA 6.0 ± 0.01eC 10.7 ± 3.5eAB 6.0 ± 0.01eA 6.0 ± 0.01eC 64.9 ± 9.5bABC 50.0 ± 4.0cdB

10.6 ± 2.4dA 9.5 ± 0.5dAB 13.0 ± 3.6dC 15.6 ± 3.5dA 20.3 ± 8.7dA 11.6 ± 4.4dB 79.7 ± 9.5aA 69.3 ± 3.1abB 8.2 ± 0.9dAB 11.0 ± 3.0dAB 8.9 ± 0.2dA 8.6 ± 0.5dB 66.0 ± 5.3bcAB 55.2 ± 3.7cAB

9.3 ± 3.5fgA 8.9 ± 0.8fgAB 20.5 ± 1.5deAB 8.8 ± 0.3fgC 6.0 ± 0.01gB 10.9 ± 0.9fgB 35.9 ± 4.1cD 69.6 ± 0.4aB 8.8 ± 0.3fA 11.8 ± 0.3efgA 9.0 ± 3.0fgA 15.3 ± 1.5efA 49.5 ± 8.5bCD 28.1 ± 1.8cdC

7.7 ± 1.5efA 7.2 ± 2.1efB 12.3 ± 2.1deC 14.8 ± 1.1dAB 7.6 ± 0.5efB 6.0 ± 0.01fB 82.5 ± 2.5bA 90.0 ± 0.01aA 7.2 ± 0.7efBC 9.0 ± 0.01efAB 7.6 ± 1.5efA 8.5 ± 0.3efB 57.7 ± 2.3cBCD 54.0 ± 4.0cAB

10.3 ± 0.6efA 8.0 ± 1.0fgB 27.5 ± 2.5dA 10.7 ± 0.6efABC 11.5 ± 0.5eAB 8.7 ± 0.6efgB 77.1 ± 2.0bAB 90.0 ± 0.01aA 6.0 ± 0.01gC 6.0 ± 0.01gB 6.3 ± 0.6gA 6.8 ± 0.7gBC 79.0 ± 1.0bA 59.8 ± 1.7cA

9.9 ± 0.9efA 7.7 ± 0.6fgB 22.5 ± 1.5dAB 12.1 ± 1.0eABC 7.8 ± 0.2fgB 6.0 ± 0.01gB 39.3 ± 0.6bCD 39.5 ± 0.5bC 7.2 ± 0.2fgBC 8.3 ± 0.5fgAB 6.0 ± 0.01gA 6.3 ± 0.6gC 42.7 ± 2.3aD 26.1 ± 1.0cC

Mean values in the same column that do not share the same small superscript letter and in the same row that do not share the same capitalized superscript letter are significantly different (p b 0.001 for columns; p b 0.05 for rows).

Izmir oreganos; E. coli O157:H7 most by Turkish and Izmir oreganos, Cinnamon, and thyme; and K. oxytoca most by thyme only. Out of the six plant essential oils—citrus (Citrus lemon), olive (Olea europaea), ajwain (Trachiyspirum ammi), almond (Amygdalus communis), Bavchi (Psoralea corylifolia) and neem (Azadirachta indica)—tested against the five Gram-positive bacteria (Lactobacillus acidophilus, Streptococcus pneumoniae, S. aureus, Micrococcus luteus, and Bacillus cereus) and the two Gram-negative bacteria (Klebsiella pneumonia, and E. coli), the most influential antibacterial effects were shown to belong to almond and neem essential oils (Upadhyay et al., 2010). Stepwise selection showed that MLR models as a function of essential oil type elucidated variation in mean inhibition data of all the Gram-negative and -positive bacteria better than did the best-fit MNLR models except for K. oxytoca (Table 5). In accounting for variation in inhibition data, the best-fit MLR models had R2 values that vary between 97.5% for CNS and S. aureus and 99.9% for E. coli O157:H7. The cross-validation-based predictive power (R2CV) of the best-fit

M(N)LR models ranged from of 94.4% for CNS to 99.8% for E. coli O157:H7. The best-fit M(N)LR models indicated that regardless of the Gram-negative versus -positive bacteria, the essential oils of Turkish, Istanbul and Izmir oreganos, cinnamon, and thyme had consistently higher inhibitory effects, while orange peel essential oil had consistently a lower inhibitory effect than anise essential oil as the reference level of the categorical explanatory variable of the essential oil type. When all the M(N)LR models of inhibition of both the Gram-negative and -positive bacteria were considered, the maximum (61 ± 16 mm) and minimum (−3.9 ± 4.5 mm) mean inhibition relative to the reference level of anise occurred with Izmir oregano and orange peel essential oils, respectively. The highest and lowest variability in inhibition relative to anise essential oil was observed for the Gram-positive bacteria by thyme (SD = 26 mm), and myrtus (SD = 3.5 mm) and for the Gram-negative bacteria by Istanbul oregano (SD = 20 mm), and orange peel (SD = 1.6), respectively. As for the best-fit MNLR model of inhibition of K. oxytoca, the inclusion of AOC, PSC, and their interaction

Table 5 Rates of change in inhibition (mm) of Gram-negative and -positive bacteria as a function of plant essential oil, antioxidant capacity (AOC), phenolic substance content (PSC), and interaction term between AOC and PSC based on the best-fit multiple linear and non-linear regression models (n = 42). Gram-positive bacteria L. innocua Intercept

9.0

CNS 15.6

Essential oil type (Anise as reference) Bay leaves −3.0 −8.1 Cinnamon 12.3 5.5 Clove 5.8 −2.5 Fennel −0.67 −5.5 Hop 20.6 −9.6 Istanbul oregano 46.6 12.0 Izmir oregano 60.0 61.2 Mint −1.0 5.8 Myrtus −1.6 0.73 −0.8 −8.3 Orange peel Sage 1.63 −5.3 Thyme 54.6 34.2 Turkish oregano 45.0 54.6 AOC (%) PSC (mg/L GAE) AOC*PSC SE (mm) 1.2 4.3 99.8 97.5 R2 (%) R2adj (%) 99.5 94.4 R2CV (%) D-W 3.1 2.9 VIF b2 b2

Gram-negative bacteria S. aureus 23.3 −12.5 27.8 −12.3 −15.0 1.0 26.6 48.3 −11.6 −7.5 −14.8 −9.2 20.3 21.2

B. subtilis 9.2

Y. enterocolitica 8.6

S. Enteritidis

S. Typhimurium

P. mirabilis

E. coli O157:H7

10.6

9.3

7.6

10.3

−3.2 18.6 2.8 −2.6 −1.3 58.3 43.8 0.01 −3.2 −3.2 4.0 80.8 33.1

3.0 9.2 1.0 −2.6 28.4 49.6 81.3 −2.6 2.0 −2.6 −2.6 56.2 41.3

−1.1 2.4 4.9 9.7 0.97 69.0 58.7 −2.4 0.40 −1.7 −2.0 55.4 44.6

−0.47 11.2 −0.53 −3.3 1.5 26.5 60.2 −0.53 2.4 −0.33 6.0 40.1 18.8

−0.47 4.6 7.1 −0.07 −1.6 74.8 82.3 −0.47 1.3 −0.07 0.8 50.0 46.3

−2.3 17.1 0.33 1.1 −1.6 66.7 79.6 −4.3 −4.3 −4.0 −3.5 68.6 49.4

3.8 97.5

3.6 98.7

4.8 97.8

4.4 98.0

2.9 98.2

1.7 99.7

1.1 99.9

94.5 2.6 b2

97.1 2.7 b2

95.1 3.1 b2

95.6 2.8 b2

96.1 2.9 b2

99.4 2.7 b2

99.8 2.9 b2

K. oxytoca −49.2 −3.9 11.8 2.7 −1.4 −2.8 33.9 35.3 0.09 −0.77 −3.1 −3.2 35.1 17.5 0.91 8.5 −0.13 0.8 99.5 99.2 2.9 N10

CNS: coagulase-negative staphylococci; SE: standard error; D-W: Durbin–Watson statistic; and VIF: variance inflation factor (alpha-to-enter and -to-remove values = 0.05) (p b 0.05).

40

G. Akdemir Evrendilek / International Journal of Food Microbiology 202 (2015) 35–41

relationship was found to be significant, at a rate of a 0.9-mm or 8.5-mm increase in inhibition per a one-unit increase in AOC (%) or PSC (mg/L GAE), respectively, and at a rate of a 0.13-mm decrease in inhibition per a one-unit increase in the interaction term when all the other terms were held constant (p b 0.05). Table 6 shows that R2adj and R2CV values of the best-fit MLR models of all the bacterial inhibition as a function of the fractional compound composition ranged from 93.4% and 92.4% for CNS to 99.5% and 99.3% for P. mirabilis, respectively. Out of a total of the 65 compounds, 24 compounds were selected by the best-fit MLR models. Out of 24 compounds, the three most frequent ones were α-terpinene (90%) (positively correlated with the bacterial inhibition except for S. Enteriditis), p-cymene (60%) (positively correlated with the bacterial inhibition except for CNS), and terpinolene (50%) (negatively correlated with the bacterial inhibition). Out of the three most frequent compounds, terpinolene was most influential on the bacterial inhibition given the magnitude of its associated rates of change. The number of compounds in the best-fit MLR models varied between three (α-terpinene, thymol, and β-bisabolene) for S. Enteriditis and seven (1,8-cineole, α-terpinene, terpinolene, p-cymene, (E)-cinnamaldehyde, β-myrcene, and camphore) for E. coli O157:H7, and (α-terpinene, methyl chavicol, trans-cinnamaldehyde, p-cymene, caryophyllene oxide, eugenol, and bornyl acetate) for K. oxytoca. 1,8-cineole, and α-thujone were the only two plant essential components common between the two bestfit MLR models of AOC and PSC with the high R2adj and R2CV values. The best-fit MLR model of AOC included α-terpinene, terpinolene, 1,8cineole, cinnamyl acetate, eugenyl acetate, α-thujone, piperitone

oxide, and neryl acetate, whereas that of PSC included p-cymene, 1,8-cineole, α-terpineol, trans-cinnamaldehyde, methyl chavicol, α-thujone, linalool, Δ-cadinene, and β-selinene.

4. Conclusions The present study indicated that Izmir oregano essential oil out of the 14 essential oils exhibited the most inhibitory effect, while the minimum inhibitory impact belonged to orange peel, regardless of the bacteria type. The most inhibitory compounds that are correlated positively and negatively with the bacterial inhibition were found to be β-bisabolene (Turkish and Istanbul oreganos) and terpinolene (thyme), respectively. Essential oils of oregano and thyme species presented the highest inhibitory effects against both Gram-positive and Gram-negative bacteria and also had higher AOC and PSC. A significant relationship was found to exist among AOC, PSC, and antibacterial effects of the plant essential oils in the present study. Inhibitory effects of plant essential oils by disk diffusion assay are known to depend on the presence and activity of antimicrobial compounds, and their diffusivity, and thus, compounds with higher diffusivity are likely to show better inhibitory effects. Diffusivity of the tested compounds is not taken into consideration in this study; therefore, it is suggested to determine in future studies the correlation between the diffusivity and antimicrobial effects of compounds found in plant essential oils.

Table 6 Rates of change in antioxidant capacity (AOC), phenolic substance content (PSC), and inactivation (mm) of Gram-negative and -positive bacteria as a function of fractional compound composition (%) of plant essential oils based on the best-fit multiple linear regression models (n = 42). AOC (%)

Intercept 66.4 1,8-cineole 0.10 α-terpinene 1.8 Cinnamyl acetate 4.0 Eugenyl acetate 0.24 α-thujone −0.18 Piperitone oxide 1.6 Neryl acetate 4.0 Terpinolene −63.4 Linalool Methyl chavicol α-terpineol Trans-cinnamaldehyde p-cymene Δ-cadinene β-selinene Terpinen-4-ol α -copaene Camphene α-terpinene-1 Borneol (E)-cinnamaldehyde β-farnesene Carvacrylmethyl ether Thymol β-bisabolene Caryophyllene oxide β-myrcene Camphore Eugenol Bornyl acetate SE 0.9 98.6 R2adj (%) 2 98.2 R CV (%) D-W 1.5 VIF b3

PSC Gram-positive bacteria Gram-negative bacteria (mg/LGAE) L. innocua CNS S. aureus B. subtilis Y. enterocolitica S. Enteritidis S. Thyphimurium P. mirabilis E. coli O157:H7 6.7 −0.03

10.2 −0.79 4.7

13.6

9.3

7.3

7.4

12.5

7.7

7.3

4.6

2.2

6.2

−4.3

2.0 8.8

6.0

9.1 −0.11 5.5

K. oxytoca 6.9 1.1

4.3 −3.1

−0.04

−138.3 0.07 −0.2 0.03 −0.04 0.12 1.9 0.14

−313.9

−222.2

−248.5

−202.0 0.32

0.63 1.9

−3.0

12.2 6.3

1.6

1.4

0.99

6.5

1.9

0.48 1.9

9.0 −7.7

−9.5 −1.0 48.6 0.6 2.2

0.29 21.2 2.1 337.1 47.2

8.8 −2.9 −0.53

0.2 97.4 96.8 2.2 b2

2.9 98.3 97.9 1.2 b25

5.9 93.4 92.4 1.6 b6

4.6 94.7 93.7 1.2 b3

4.0 97.7 96.6 2.0 b5

5.9 95.2 93.4 2.4 b3

5.4 95.7 94.3 2.2 b49

3.5 96.4 95.3 2.0 b3

2.0 99.5 99.3 2.1 b3

2.3 99.4 99.1 1.7 b6

−0.06 −1.1 1.1 99.3 99.0 2.3 b5

CNS: coagulase-negative staphylococci; SE: standard error; D–W: Durbin–Watson statistic; and VIF: variance inflation factor (alpha-to-enter and -to-remove values = 0.001) (p b 0.001).

G. Akdemir Evrendilek / International Journal of Food Microbiology 202 (2015) 35–41

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Empirical prediction and validation of antibacterial inhibitory effects of various plant essential oils on common pathogenic bacteria.

In this study, fractional compound composition, antioxidant capacity, and phenolic substance content of 14 plant essential oils-anise (Pimpinella anis...
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